(Insecta: Diptera) from a Stream in the Floresta Da Tijuca, Rio De Janeiro, Brazil

FEEDING HABITS OF CHIRONOMID LARVAE 269

FEEDING HABITS OF CHIRONOMID LARVAE (INSECTA: DIPTERA) FROM A STREAM IN THE FLORESTA DA TIJUCA, RIO DE JANEIRO, BRAZIL

HENRIQUES-OLIVEIRA, A. L.,1 NESSIMIAN, J. L.1 and DORVILLÉ, L. F. M.2 1Departamento de Zoologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil 2Faculdade de Formação de Professores, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazil Correspondence to: Ana Lucia Henriques de Oliveira, Laboratório de Entomologia, Depto. de Zoologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro, C.P. 68044, CEP 21944-970, Cidade Universitária, Rio de Janeiro, RJ, Brazil, e-mail: [email protected] Received January 14, 2002 – Accepted April 29, 2002 – Distributed May 31, 2003 (With 2 figures)

ABSTRACT

Chironomids larvae are frequently one of the most abundant and diverse groups of insects in several kinds of aquatic environments. Also, they play a major role in the aquatic food webs, representing a major link among producers and secondary consumers. This work investigates the feeding behavior of the chironomid larvae present in the Rio da Fazenda, situated in the Parque Nacional da Tijuca, Rio de Janeiro, Bra- zil, between August 1994 and May 1995. Algae, fungi, pollen, leaf and wood fragments, animal remains, detritus and silt were the main gut contents found in the larvae studied. The main food item ingested by the larvae was detritus, except for the Stenochironomus whose main food source was leaf and wood fragments. Tanypodinae exhibited a large quantity of animal remains of several kinds in the diet. During the period studied it was observed that the diet of 16 genera (out of 24 studied) varied. Tanypodinae had mainly coarse particulate organic matter (> 1 mm) in the gut contents, while Chironominae and Orthocladiinae had fine particulate organic matter (< 1 mm). Key words: food habits, gut contents, Chironomidae, larvae.

RESUMO

Hábitos alimentares das larvas de Chironomidae (Insecta: Diptera) de um riacho na Floresta da Tijuca, Rio de Janeiro, Brasil As larvas de Chironomidae são freqüentemente o grupo de insetos mais abundante e diversificado em vários tipos de ambientes aquáticos, apresentando importante papel nas redes tróficas das comunidades aquáticas, por constituírem efetiva ligação entre produtores e consumidores. Este trabalho analisou o comportamento alimentar das larvas de Chironomidae presentes no rio da Fazenda, localizado no Parque Nacional da Tijuca, Rio de Janeiro, Brasil, entre agosto de 1994 e maio de 1995. Os principais itens alimentares encontrados foram algas, fungos, pólen, fragmentos vegetais, restos animais, detritos e silte. O principal item alimentar ingerido pelas larvas foi detrito, exceto para Stenochironomus, cujo principal componente alimentar foram fragmentos vegetais. Os Tanypodinae também exibiram grande quantidade de restos animais de diversos grupos na dieta alimentar. Foi observada variação na dieta alimentar para 16 gêneros. Os Tanypodinae apresentaram principalmente matéria orgânica particulada grossa (> 1 mm) no conteúdo digestivo, enquanto os Chironominae e os Orthocladiinae apresentaram matéria orgânica particulada fina (< 1 mm). Palavras-chave: alimentação, conteúdo estomacal, Chironomidae, larva.

Braz. J. Biol., 63(2): 269-281, 2003 270 HENRIQUES-OLIVEIRA, A. L., NESSIMIAN, J. L. and DORVILLÉ, L. F. M.

INTRODUCTION particle filterers in suspension or deposited material gatherers. Throughout all the subfamilies registered Organic matter found in flowing waters co- this is the most common feeding process among mes from the aquatic photosynthesis and mainly from chironomids (Oliver, 1971). terrestrial sources (Hirabayashi & Wotton, 1998). Scrapers are especially adapted to remove Both allochthonous (leaves, flowers, fruits and twigs) firmly attached algae in the exposed surfaces placed and autochthonous detritus support the stream biota in flowing waters, sediments, and submerged organic by providing it an available food supply. Several matter. Predators (engulfers and piercers) are works on aquatic insects have shown their role in commonly represented by individuals from the the decomposition processes of allocthonous material Tanypodinae subfamily and feed on living animal and nutrient cycling (e.g., Cummins, 1973, 1974; tissue, frequently higher than 1 mm. Engulfers Merritt et al., 1984). According to Cummins (1973), usually attack and ingest the whole prey or its pieces, a significant portion of material cycling and energy while piercers bore the prey tissues removing their flow in freshwater ecosystems involve various forms body fluids (Berg, 1995). However, it is important of organic matter processing by invertebrates. to recognize that most chironomids are not restricted Chironomids have an important role in the food to a single feeding mode, as also pointed out by webs of aquatic communities, representing a ma- Nessimian & Sanseverino (1998) and Nessimian jor link between producers and secondary consumers et al. (1999). (Tokeshi, 1995). Chironomid larvae are opportunistic The present work aims to study and analyze omnivorous, ingesting a wide variety of food items the feeding habits of chironomid larvae present in (Cummins & Klug, 1979). Generally, these larvae the rithral section of the Rio da Fazenda (Fazen- ingest five kinds of food: algae, detritus and da River), in the Parque Nacional da Tijuca (Tijuca associated microorganisms, macrophytes, wood National Park), Rio de Janeiro, Brazil. debris, and invertebrates (Berg, 1995). Based upon the feeding mode, larvae can be MATERIALS AND METHODS grouped in six categories: collectors (gatherers and filterers), shredders, scrapers, and predators (engul- Study area fers and piercers) (Coffman & Ferrington, 1996). The study area is located in a 1st order section According to the classification scheme of functional of the Rio da Fazenda (also called Rio Humaitá), feeding groups based upon feeding mode and general a small stony stream that flows in the Parque Na- detritus particle size (Cummins, 1973, 1974), food cional da Tijuca. This area is completely surrounded items can be grouped in the following categories: by the urban perimeter of the city of Rio de Janeiro coarse particulated organic matter (CPOM – > 1 (Drummond, 1997), between 22o55’S and 23o00’S mm), such as leaves from the riverine vegetation and 43o11’W and 43o19’W, with an area of and macrophytes; fine particulated organic matter approximately 32 km2 of tropical forests. This (FPOM – > 0.5 µm < 1 mm), from a great variety vegetation was greatly modified by human activities, of resources including CPOM fragmentation, peri- especially coffee plantations, being the result of a phyton, algae, and microorganisms; and dissolved reforestation program dated from the second half organic matter (DOM – < 0.5 µm). of the nineteenth century. Therefore, shredders ingest particles larger than The collecting site is located at 400 m a.m.s.l. 1 mm, feeding on CPOM (vascular plants, macro- and the stream is on average 2 m wide and 20 cm algae, wood and submerged leaves) and collectors deep. At the time of the study period the stream was and scrapers ingest particles smaller than 1 mm. almost completely covered by riverine vegetation, Collectors feed on FPOM and are named this way with little direct sunlight exposure and mosses because of the reaggregation of the small particles covered many stones, thus the distinction between resulting from their ingesting activities, being either riffle and pool areas was not very clear.

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Procedures fragments, and fungi were common in the majority Chironomid larvae were collected by means of the Chironominae and Orthocladiinae genera of a Surber net (900 cm2 area and 350 µm mesh size) (Tables 2 and 3). Stenochironomus was the only in August (winter) and November (spring) 1994, genus that did not show detritus as its major and in February (summer) and May (autumn) 1995. component in the diet. Instead of that, this genus The sampled larvae were preserved in 80% ethanol presented leaf and wood fragments as its main food and sorted in morphotypes under the stereoscopic source (Fig. 1). The Tanypodinae diet (Table 1) also microscope. The identification up to generic level included several components of animal origin, which was done with the aid of the taxonomic keys of many times came to represent more than 50% of Cranston et al. (1983), Epler (1995), Pinder & Reiss the diet of some genera. (1983), Trivinho-Strixino & Strixino (1995) and The mean contributions of each food item some taxonomic descriptions. registered for each taxon are shown in Table 4, and Gut content analysis was based on the each subfamilies among the months studied are observations of the gut contents of previously slide represented in the Fig. 2. Algae were more important mounted larvae, under a microscope (1000x). in the diet of the larvae studied in the winter and Monthly an average of five specimens of each taxon autumn for Chironominae and Orthocladiinae, while collected were analyzed, amounting to 440 leaf and wood fragments were more common in the individuals in 24 taxa (some taxa does not have diet of the Chironominae. specimens in all season). All food items were Pollen was the component that showed the smallest identified and measured by means of an eyepiece participation in the diets, being represented in the spring micrometer scale (400x). and summer. Animal remains had the highest The percentage of each item was estimated participation in the Tanypodinae diet in individuals to the subfamilies in each season and to the genera analyzed in November and February (Fig. 2). during the period studied, as well as the maximum The results of the Chi-square test showed that size (in micrometers) of the ingested particles. The the diet of 16 genera showed some variation according arithmetic mean and the standard deviation were to the month studied. Only Chironomus, aff. Omisus, calculated with base on the percentage of the item Rheotanytarsus, Stempellinella, Tanytarsus, Chiro- ingested for all individuals of each genera. nomini sp. 1, Lopescladius, and Thienemanniella did In order to evaluate if there was a significant not show variation in the diet (Table 5). change in the diet of the chironomid larvae, the Chi- Regarding the maximum size of the food items Square (X2) test was used with 18 degrees of freedom ingested by the larvae, according to the classification for each genus, based on the relative participation proposed by Cummins (1974), the biggest particle of each food item in each taxon collected monthly. size ingested was found in cf. Djalmabatista, mainly Significant values were accepted for p < 0.05. in the specimens analyzed in February (2,875 µm), and the smallest was found in Thienemanniella, mainly µ RESULTS in the specimens analyzed in May (5 m). According to Cummins (1974), Ablabesmyia, cf. Djalmabatista, Algae, fungi, pollen, leaf and wood fragments aff. Larsia, and aff. Pentaneura, from the subfamily and fibers, animal remains, particulated organic Tanypodinae, presented coarse particulated organic matter (detritus), and silt were the main components matter (CPOM > 1000 mm) in the gut contents in found in the gut content analysis (Fig. 1). The food at least one season. Labrundinia was the only genus items registered for each genus, as well as their major from this subfamily that presented fine particulate contributions, can be seen in Tables 1 to 3. Detritus organic matter (FPOM > 0.5 µm < 1 mm) in its guts was the most ingested food item by the majority of contents. Chironominae and Orthocladiinae genera the studied genera. Besides that, algae, leaf and wood exhibited FPOM in its guts contents.

Braz. J. Biol., 63(2): 269-281, 2003 272 HENRIQUES-OLIVEIRA, A. L., NESSIMIAN, J. L. and DORVILLÉ, L. F. M.

Tanypodinae 100% Sil 80% Det

60% Ani LW 40% Pol Fun 20% Alg

0% Abl Dja Lab Lar Pen

Chironominae 100% Sil 80% Det

60% Ani LW 40% Pol Fun 20% Alg

0% Chi End Nil Omi Pha Pol

Chironominae 100% Sil 80% Det

60% Ani LW 40% Pol Fun 20% Alg

0% Rhe Stp Stc Tan Tri Ch1

Orthocladiinae 100% Sil 80% Det

60% Ani LW 40% Pol Fun 20% Alg

0% Cor Lop Nan Pak Par Pse Thi

Fig. 1 — Relative composition of the food items observed in the gut contents of the chironomid larvae, for each season, in Rio da Fazenda, Parque Nacional da Tijuca, Rio de Janeiro, Brazil. Alg – algae; Fung – fungi; Pol – pollen; LW – leaf and wood fragments; Ani – animal remains; Det – detritus; Sil – silt. Abl –Ablabesmyia, Dja – cf. Djalmabatista , Lab – Labrundinia, Lar – aff. Larsia, Pen – aff. Pentaneura, Chi – Chironomus, End – Endotribelos, Nil – Nilothauma, Omi – aff. Omisus, Pha – Phaenopsectra, Pol – Polypedilum, Rhe – Rheotanytarsus, Stp – Stempellinella, Stc – Stenochironomus, Tan – Tanytarsus, Tri – aff. Tribelos, Ch1 – Chironomini tipo 1, Cor – Corynoneura, Lop – Lopescladius, Nan – Nanocladius, Pak – aff. Parakiefferiella, Par – Parametriocnemus, Pse – Pseudosmittia, and Thi – Thienemanniella.

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TABLE 1 Food items observed in the gut contents of members of the subfamily Tanypodinae at Rio da Fazenda, Parque Nacional da Tijuca, RJ, between August 1994 and May 1995.

Main food items and their Taxa Food items Sizes higher percentage Chlorophyceae: filamentous and unicellular algae Desmidiaceae (Cosmarium) Fungi (conidia) Detritus – 78% August Max. – 1050 µm Ablabesmyia Leaf and wood fragments and detritus Animal remains – 48% May Min. – 50 µm Animal remains: Chironomids larvae (Endotribelos, Pseudosmittia, Stenochironomus), Cladocera Pollens (several types) and spores Chlorophyceae: filamentous, unicellular, and colonial algae (Mougeotia?) Detritus – 57% November Desmidiaceae (Cosmarium) and May Fungi (conidia) Max. – 2875 µm Animal remains – 50.7% Leaf and wood fragments and detritus cf. Djalmabatista Min. – 50 µm February Animal remains: Chironomids larvae Algae – 9% August (Lopescladius, Tanypodinae and Tanytarsini) Copepoda (nauplius), Oligochaeta setae Pollens (several types) and spores Chlorophyceae: filamentous, unicellular, and colonial algae (Spyrogira) Detritus – 90% May Cyanophyceae (Anabaena?) Max. – 200 µm Labrundinia Pollen – 10.6% February Desmidiaceae (Cosmarium, Staurastrum) Min. – 12.5 µm in Algae – 7% November Fungi (conidia and hyphas) detritus Pollens (several types) and spores Chlorophyceae: filamentous and unicellular algae Detritus – 74.5% May Desmidiaceae (Cosmarium) Animal remains – 22.7% Diatomaceae Max. – 1865 µm aff. Larsia February Fungi (conidia and hyphas), detritus Min. – 20 µm Algae – 14.4% November Animal remains: chironomid larvae, Copepoda, Cladocera Pollens (several types) and spores Chlorophyceae: filamentous, unicellular, and colonial algae Desmidiaceae (Cosmarium, Micrasteria) Detritus – 69.7% May Dinophyceae Max. – 1912 µm aff. Pentaneura Animal remains – 46.4% Fungi (conidia and hyphas), detritus Min. – 25 µm November Animal remains: Chironomids larvae Copepoda, Cladocera Pollens (several types) and spores

Braz. J. Biol., 63(2): 269-281, 2003 274 HENRIQUES-OLIVEIRA, A. L., NESSIMIAN, J. L. and DORVILLÉ, L. F. M.

Tanypodinae 100% Sil 80% Det

60% Ani LW 40% Pol Fun 20% Alg

0% Abl Dja Lab Lar Pen

Chironominae 100% Sil 80% Det

60% Ani LW 40% Pol Fun 20% Alg

0% Chi End Nil Omi Pha Pol

Chironominae 100% Sil 80% Det

60% Ani LW 40% Pol Fun 20% Alg

0% Rhe Stp Stc Tan Tri Ch1

Orthocladiinae 100% Sil 80% Det

60% Ani LW 40% Pol Fun 20% Alg

0% Cor Lop Nan Pak Par Pse Thi

Fig. 2 — Relative composition of the food items observed in the gut contents of the chironomids subfamilies, for each season, in Rio da Fazenda, Parque Nacional da Tijuca, Rio de Janeiro, Brazil. Alg – algae; Fung – fungi; Pol – pollen; LW – leaf and wood fragments; Ani – animal remains; Det – detritus; and Sil – silt (W – winter; S – spring; Su – summer; A – autumn).

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TABLE 2 Food items observed in the gut contents of members of the subfamily chironominae at Rio da Fazenda, Parque Nacional da Tijuca, RJ, between August 1994 and May 1995.

Main food items and their Taxa Food items Sizes higher percentage Chlorophyceae: several types Cyanophyceae (Anabaena?) Detritus – 88% November Desmidiaceae (Micrasteria, Staurastrum) Leaf and wood fragments – Max. – 400 µm Chironomus Diatomaceae, Dinophyceae 12.6% February Min. – 62 µm Fungi (conidia and hyphas) Algae – 4.3% February Leaf and wood fragments and detritus Pollens (several types) and Spores Chlorophyceae: colonial and unicellular Detritus – 95.8% May algae Algae – 10.9% August Desmidiaceae (Cosmarium) Max. – 187.5 µm Endotribelos Leaf and wood fragments – Fungi (conidia and hyphas) Min. – 15 µm 19% August Leaf and wood fragments and detritus Fungi – 14% November Pollens (several types) and Spores Chlorophyceae: unicellular algae Detritus – 84% February Desmidiaceae (Micrasteria) Algae – 7% November Diatomaceae Max. – 62.5 µm Nilothauma Fungi – 100% August Fungi (hyphas) Min. – 7.5 µm Leaf and wood fragments – Leaf and wood fragments and detritus 12% May Pollens (several types) and spores Chlorophyceae: (Mougeotia?, Phycopeltis? and Spyrogira); filamentous and unicellular algae Detritus – 90.3% August Cyanophyceae (Anabaena?) Max. – 175 µm aff. Omisus Leaf and wood fragments – Desmidiaceae (Cosmarium) Min. – 25 µm 5.75% May Diatomaceae Fungi (conidia and hyphas) Leaf and wood fragments and detritus Pollens (several types) Chlorophyceae: (Mougeotia?) filamentous and unicellular algae Detritus – 88,8%August Desmidiaceae (Cosmarium and Leaf and wood fragments – Staurastrum) Max. – 400 µm Phaenopsectra 32.7% November Diatomaceae Min. – 12.5 µm Algae – 8.6% November Fungi (conidia and hyphas) Leaf and wood fragments and detritus Pollens (several types) and spores Chlorophyceae: (Mougeotia? and Spyrogira) filamentous, unicellular, and colonial algae Detritus – 88% May Cyanophyceae (Anabaena?) Algae – 18,7% August Desmidiaceae (Cosmarium and Max. – 175 µm Polypedilum Leaf and wood fragments – Staurastrum) Min. – 12.5 µm 10% May Diatomaceae, Dinophyceae Fungi (conidia and hyphas) Leaf and wood fragments and detritus Pollens (several types) and spores

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TABLE 2 (Continued.)

Main food items and Taxa Food items Sizes their higher percentage Chlorophyceae: filamentous and unicellular algae Detritus – May 93.3% Desmidiaceae (Cosmarium) Max. – 67.5 µm Rheotanytarsus Fungi – November 6.2% Diatomaceae Min. – 12.5 µm Pollen – February 3.4% Fungi (conidia and hyphas) Leaf and wood fragments and detritus Pollens (several types) and spores Chlorophyceae: filamentous and unicellular algae Desmidiaceae (Micrasteria) Detritus – May 94.4% Max. – 67.5 µm Stempellinella Diatomaceae Fungi – August 6.4% Min. – 12.5 µm Fungi (conidia and hyphas) Leaf and wood fragments and detritus Pollens (several types) and spores Chlorophyceae: filamentous, unicellular, Leaf and wood fragments – and colonial algae (Mougeotia? and February 93.71% Spyrogira) Max. – 1000 µm Stenochironomus Algae – May 14.5% Desmidiaceae (Micrasteria) Min. – 30 µm Detritus – November Fungi (hyphas) 15.2% Leaf and wood fragments and detritus Chlorophyceae: filamentous, unicellular, and colonial algae Detritus – May 93.6% Cyanophyceae (Anabaena?) Max. – 100 µm Leaf and wood fragments – Tanytarsus Desmidiaceae (Cosmarium) Min. – 12 µm August 3.5% Fungi (conidia) Leaf and wood fragments and detritus Pollens (several types) and spores Chlorophyceae: filamentous and unicellular algae (Mougeotia?; Spyrogira; Detritus – February 88.3% Phycopeltis?) Leaf and wood fragments – Desmidiaceae (Cosmarium, Micrasteria) Max. – 475 µm aff. Tribelos May 26.1% Diatomaceae Min. – 25 µm Fungi – November 5.8% Fungi (conidia and hyphas) Algae – November 3.6% Leaf and wood fragments and detritus Pollens (several types) Chlorophyceae: filamentous and unicellular algae (Spyrogira) Detritus – February 90.6% Desmidiaceae (Cosmarium, Micrasteria Algae – August 14.8% and Staurastrum) Max. – 100 µm Chironomini sp. 1 Leaf and wood fragments – Diatomaceae Min. – 12.5 µm August 4.3% Fungi (conidia and hyphas) Leaf and wood fragments and detritus Pollens (several types) and spores

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TABLE 3 Food habit observed in the gut contents of members of the subfamily Orthocladiinae at Rio da Fazenda, Parque Nacional da Tijuca, RJ, between August 1994 and May 1995.

Main food items and Taxa Food items Sizes their higher percentage Detritus – 97% February Chlorophyceae: unicellular algae Fungi – 5% August Max. – 75 µm Corynoneura Fungi (conidia and hyphas) Leaf and wood Min. – 12.5 µm Pollens (several types) fragments – 5% August Fungi (conidia and hyphas) Detritus – 97% August Max. – 31.25 µm Lopescladius Leaf and wood fragments and detritus Pollen – 2.5% February Min. – 12.5 µm Pollens (several types) Chlorophyceae: filamentous and Detritus – 89.7% February colonial algae Algae – 15.7% August Diatomaceae Max. – 90 µm Nanocladius Fungi – 12% August Fungi (conidia and hyphas) Min. – 12.5 µm Pollen – 3.3% February Leaf and wood fragments and detritus Pollens (several types) and spores

Chlorophyceae: colonial, filamentous and unicellular algae Detritus – 88.3% August Cyanophyceae (Anabaena?) Max. – 100 µm Algae – 10% May aff. Parakiefferiella Diatomaceae Min. – 12.5 µm Fungi – 16.5% February Fungi (conidia and hyphas) Leaf and wood fragments and detritus Pollens (several types)

Chlorophyceae: filamentous and unicellular algae Detritus – 90.5% Cyanophyceae (Anabaena?) November Desmidiaceae (Cosmarium) Leaf and wood fragments – Max. – 400 µm Parametriocnemus Diatomaceae 21.8% February Min. – 20 µm Fungi (conidia and hyphas) Algae – 4.6%August Leaf and wood fragments and detritus Pollens (several types) and spores Oligochaeta? Detritus – 86.1% Chlorophyceae: filamentous and November unicellular algae Max. – 87 µm Pseudosmittia Leaf and wood fragments – Fungi (conidia and hyphas) Min. – 12.5 µm 34.5% February Leaf and wood fragments and detritus Fungi – 7.6% November Pollens (several types) and spores Chlorophyceae: colonial, filamentous Detritus – 92.7% May and unicellular algae Algae – 5.4% August Max. – 50 µm Thienemanniella Fungi (conidia and hyphas) Fungi – 4.4% November Min. – 5 µm Leaf and wood fragments and detritus Pollen – 3.7% November Pollens (several types) and spores

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TABLE 4 Average contribution of each food item for the chironomid genera studied in the Rio da Fazenda, between August 1994 and May 1995. (Mean – arithmethic mean; SD – standard deviation.)

Leaf and Animal Algae Fungi Pollen Detritus Silt wood remains Tanypodinae Mean 1.82 1.42 1.62 2.40 28.46 61.34 2.92 Ablabesmyia SD 1.37 0.73 0.80 1.99 13.05 11.93 2.68 Mean 3.04 0.94 2.18 2.15 32.29 51.72 7.68 cf. Djalmabatista SD 3.57 0.53 2.02 2.13 11.33 4.25 6.08 Mean 4.49 1.58 4.66 4.28 0.49 83.50 1.02 Labrundinia SD 1.54 1.13 3.55 5.35 0.84 4.19 1.19 Mean 5.51 1.61 1.86 2.46 16.65 70.04 1.88 aff. Larsia SD 5.22 0.87 0.56 1.23 3.50 3.83 1.67 Mean 1.13 1.41 1.28 2.20 28.16 60.03 5.78 aff. Pentaneura SD 0.80 0.82 0.52 1.00 15.22 9.54 5.55 Chironominae Mean 1.25 3.14 1.12 4.76 0.09 62.10 2.55 Chironomus SD 1.78 1.86 0.89 4.72 0.15 36.22 2.41 Mean 5.96 4.18 0.87 6.79 0.00 81.32 0.90 Endotribelos SD 5.01 5.70 0.54 7.21 0.00 11.97 0.70 Mean 3.55 29.30 1.53 6.50 0.00 59.13 0.00 aff. Nilothauma SD 6.15 41.22 1.35 6.54 0.00 34.48 0.00 Mean 1.95 2.65 1.63 3.90 0.00 88.99 0.86 aff. Omisus SD 1.03 0.88 0.24 1.72 0.00 1.29 0.71 Mean 4.26 1.40 1.51 11.41 0.14 55.36 0.92 Phaenopsectra SD 3.86 1.24 0.97 12.60 0.14 34.09 0.58 Mean 7.45 3.82 1.70 7.12 0.00 79.04 0.88 Polypedilum SD 7.01 1.79 0.71 2.55 0.00 8.86 0.81 Mean 1.65 2.64 2.27 0.95 0.00 90.67 1.83 Rheotanytarsus SD 0.96 2.09 0.96 0.39 0.00 2.10 1.11 Mean 0.89 3.53 1.53 1.97 0.00 91.02 1.07 Stempellinella SD 0.67 1.79 0.62 0.66 0.00 2.38 0.42 Mean 8.03 0.13 0.05 87.23 0.00 4.57 0.00 Stenochironomus SD 4.16 0.13 0.09 6.41 0.00 6.27 0.00 Mean 1.15 1.86 1.63 2.32 0.00 91.93 1.12 Tanytarsus SD 0.37 0.45 0.62 0.84 0.00 1.28 0.60 Mean 3.07 1.96 1.30 13.45 0.00 79.11 1.12 aff. Tribelos SD 0.52 2.33 0.61 9.49 0.00 7.43 0.66 Mean 7.57 2.15 1.39 3.85 0.04 83.95 1.05 Chironomini tipo 1 SD 5.99 1.30 0.48 0.79 0.06 5.25 0.42 Orthocladiinae Mean 0.40 2.20 1.93 1.34 0.00 92.46 1.68 Corynoneura SD 0.69 2.09 0.70 2.12 0.00 5.13 1.80 Mean 0.00 1.12 1.79 0.52 0.00 96.07 0.50 Lopescladius SD 0.00 0.51 0.60 0.34 0.00 0.55 0.22 Mean 6.71 3.98 3.19 2.49 0.00 81.92 1.71 Nanocladius SD 5.51 4.79 0.87 1.46 0.00 7.57 0.66

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TABLE 4 (Continued.)

Leaf and Animal Algae Fungi Pollen Detritus Silt wood remains Orthocladiinae Mean 7.04 5.76 2.01 1.92 0.00 81.18 2.09 aff. Parakiefferiella SD 7.55 6.31 1.23 0.84 0.00 6.01 0.82 Mean 2.31 2.30 1.67 8.75 0.50 82.95 1.52 Parametriocnemus SD 1.53 0.93 0.15 7.87 0.61 8.52 0.47 Mean 2.06 3.57 1.80 18.77 0.00 73.15 0.66 Pseudosmittia SD 1.93 2.43 1.16 11.55 0.00 9.49 0.50 Mean 2.74 2.05 2.74 1.15 0.00 90.83 0.47 Thienemanniella SD 2.23 1.39 0.89 1.66 0.00 1.29 0.46

TABLE 5 Chi-square values found for the gut contents of chironomid larvae from the Rio da Fazenda, Parque Nacional da Tijuca, RJ, between August 1994 and May 1995 (p < 0.05).

Taxa Chi-square values (X2) Ablabesmyia 56.99 cf. Djalmabatista 70.35 Labrundinia 55.16 aff. Larsia 34.50 aff. Pentaneura 67.16 Chironomus 23.06 Endotribelos 89.11 aff. Nilothauma 386.08 aff. Omisus 6.50 Phaenopsectra 46.93 Polypedilum 41.63 Rheotanytarsus 14.02 Stempellinella 8.42 Stenochironomus 46.07 Tanytarsus 4.43 aff. Tribelos 43.67 Chironomini sp. 1 25.81 Corynoneura 36.03 Lopescladius 2.97 Nanocladius 49.38 aff. Parakiefferiella 67.61 Parametriocnemus 40.98 Pseudosmittia 51.74 Thienemanniella 23.65

Braz. J. Biol., 63(2): 269-281, 2003 280 HENRIQUES-OLIVEIRA, A. L., NESSIMIAN, J. L. and DORVILLÉ, L. F. M.

DISCUSSION to prey size and the predator’s development stage. Labrundinia was the only genus in this subfamily Gut content analysis showed that 16 out of the with non-animal material in the gut contents. This 24 chironomid genera studied in this work showed genus is reported by Nessimian et al. (1999), working a change in their feeding habits among the four in a sand dune marsh in the coast of Rio de Janeiro, months studied. This variation in the diet may suggest as feeding on animal sources (chironomid larvae, that these groups present a low degree of selectivity, Cladocera, and Copepoda), mainly in summer and having more generalist habits. According to Berg spring (dry season), and diatoms in the autumn and (1995) there are few chironomid species that present winter (rainy season). The absence of animal matter nutritional selectivity, the great majority being in the gut contents of Labrundinia larvae in the Rio generalists and opportunistic. da Fazenda might reflect the small size of the The same pattern was confirmed by Nessimian sampled individuals. This fact agrees with Oliver (1997), studying the functional categorization of (1971) and Cummins (1973), which recorded that macroinvertebrates in a sand dune marsh in Maricá larvae at different developmental stages often have (State of Rio de Janeiro) found that most species different diets. had generalist and opportunistic habits, feeding on Among Chironominae and Orthocladiinae what was available at that moment. Nessimian & larvae the greatest change was detected in Nilothauma Sanseverino (1998), studying the diet of chironomid (X2 = 386.08). This genus showed only fungi in the larvae in a stream in the mountain region of the State gut contents of the individuals analyzed in August, of Rio de Janeiro, registered that the composition while the highest diversity of items was found in of the gut contents changed according to the type the individuals analyzed in May of 1995, when of microhabitat (e.g., type of substrate) where the detritus, leaf and wood fragments, fungi, and algae larvae were found. Also, they observed differences was observed in their gut contents. Stenochironomus among samples from the same microhabitats in was the only genus, which fed mainly on leaf and different seasons, as a result of changes in the type wood fragments, feeding both on leaf cells and wood of available substrate. fibers. These larvae are considered by many authors Detritus was the main food item found in most to be truly xylophagous (e.g., Cranston & Oliver, of the larvae studied. According to Berg (1995), 1988; Berg, 1995). Epler (1995) points out that it is not unusual for this item to represent 50%-70% Stenochironomus larvae are miners of submerged of the gut contents of chironomids. Nessimian & leaves and wood fragments. Sanseverino (1998) found detritus as the most The particle analysis of the size of what was abundant item in the diet of Chironominae and ingested by the larvae revealed that, with the Orthocladiinae genera from the Paquequer River exception of the Tanypodinae, which might be (Teresópolis, State of Rio de Janeiro), together with classified as predators since they feed upon animal a high concentration of pollen and spores. In Rio material frequently higher than 1 mm, most da Fazenda, the most important items, after detritus, chironomid larvae are classified as collectors, feeding were leaf and wood fragments as well as fungi in upon fine particulate organic matter (FPOM). Also, the diet of the Chironominae and Orthocladiinae according to Cummins (1974), FPOM can be divided subfamilies, while animal remains were found in in three categories: MPOM – mean particulate Tanypodinae. organic matter, ranging from 250 to 1000 µm; The highest diversity of food items was SPOM – small particulate organic matter, ranging observed in the Tanypodinae. Several genera of this from 75 to 250 µm; and VPOM – very fine subfamily presented algae, fungi, pollen, leaf and particulate organic matter, ranging from 0.5 to 75 wood fragments, and detritus, but also many µm. According to this classification, most of the Chironominae and Orthocladiinae genera as food Chironominae and Orthocladiinae genera showed items. Pinder (1986) points out that the Tanypodinae SPOM in their gut contents. larvae have a quite diverse diet among animals and Two groups of collectors were found in the Rio plants items. The occurrence of some genera in the da Fazenda: the collector-gatherers and the collectors- gut contents of these chironomids is due to their filterers. In this latter group we can include Nilothauma, availability in the habitat and can also be related Rheotanytarsus, Corynoneura, Lopescladius, and

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Thienemanniella, which frequently ingested particles stream invertebrates. Ann. Ver. Ecol. Syst., 10: 147-172. smaller than 75 µm. CUMMINS, K. W., 1973, Trophic relations of aquatic insects. On the other hand Chironomus, Phaenopsectra, Annual Review of Entomology, 18: 183-206. aff. Tribelos, and Parametriocnemus showed MPOM CUMMINS, K. W., 1974, Structure and functions of stream in their gut contents, and might be considered besides ecosystems. Bioscience, 24: 631-641. collector-gatherers, as possible scrapers and shredders, DRUMMOND, J. A., 1997, Devastação e preservação since the capture and food ingestion can involve ambiental: os parques nacionais do Estado do Rio de Janeiro. (Coleção Antropologia e Ciência Política, 2). more than one feed mode, and in this genera leaf EDUFF, Niterói, RJ, 306p. and wood fragments, algae and other materials often µ EPLER, J. H., 1995, Identification manual for the larvae higher than 250 m were found. Stenochironomus Chironomidae (Diptera) of Florida. Department of might be considered as a true shredder, since it Environmental Protection, Division of Water Facilities, presented fibers and leaf and wood fragments as Tallahassee, 250p. the main food source. HIRABAYASHI, K. & WOTTON, R. S., 1998, Organic matter Although the functional group categories are processing by chironomid larvae (Diptera: Chironomidae). based partially in the morphology of the species, Hydrobiologia, 382: 151-159. there is considerable flexibility in the mode of MERRIT, K. W., CUMMINS, R. W. & BURTON, T. M., 1984, feeding among chironomids. Many factors, such as The role of Aquatic insects in the processing and cycling of nutrients, pp: 134-163. In: V. H. Resh & D. M. Rosenberg larval size, food quality and type of sediment might (eds.), The ecology of aquatic insects. Praeger Publishers, influence the larval feeding behavior (Berg, 1995). New York, xi + 625p. In addition to that, the change in the larval diet might NESSIMIAN, J. L. & SANSEVERINO, A. M., 1998, Trophic also reflect the differences observed in the structure functional categorization of the chironomid larvae (Diptera: of the Rio da Fazenda, which determines changes Chironomidae) in a first-order stream at the mountain region of Rio de Janeiro State, Brazil. Verh. Internat. Verein. Limnol., in the structure and composition of the substrates 26(IV): 2115-2119. regarding the quality of the available resources. NESSIMIAN, J. L., 1997, Categorização funcional de According to Nessimian & Sanseverino (1998), macroinvertebrados de um brejo de dunas no Estado do Rio changes in the feeding habits of chironomids are de Janeiro. Rev. Brasil. Biol., 57(1): 135-145. dependent, to a great extension, on environmental NESSIMIAN, J. L., SANSEVERINO, A. M. & OLIVEIRA, A. conditions. L. H., 1999, Relações tróficas de larvas de Chironomidae (Diptera) e sua importância na rede alimentar em um brejo Acknowledgments — The authors acknowledge CNPq and no litoral do Estado do Rio de Janeiro. Revta. Brasil. FAPERJ for financial support and for the grant provided to the Entomol., 43(1/2): 47-53. first author by CAPES. OLIVER, D. R., 1971, Life history of the Chironomidae. Ann. Rev. Entomol., 12: 211-230. PINDER, L. C. V. & REISS, F., 1983, The larvae of REFERENCES Chironominae (Diptera: Chironomidae) of the Holartic region. Keys and diagnoses. In: T. Wiederholm (ed.), BERG, H. B., 1995, Larval food and feeding behaviour, pp. 136- Chironomidae of the Holartic region. Keys and diagnose. 168. In: P. D. Armitage, P. S. Cranston & L. C. V. Pinder Part I: Larvae. Ent. Scan. Suppl., 19: 293-435. (eds.), The Chironomidae: biology and ecology of non-biting PINDER, L. C. V., 1986, Biology of freshwater Chironomidae. midges. Chapman & Hall, London, 584p. Ann. Rev. Entomol., 31: 1-23. COFFMAN, W. P. & FERRINGTON, L. C., 1996, Chironomidae, TOKESHI, M., 1995, Production ecology, pp: 269-296. In: P. pp: 635-754. In: K. W. Merrit & R. W. Cummins (eds.), D. Armitage, P. S. Cranston & L. C. V. Pinder. The An introduction of aquatic insects of North America. 3. ed. Chironomidae. Biology and ecology of non-biting midges. Kendall Hunt Publishing Co., Dubuque, xii + 862p. Chapman & Hall, London, 584p. CRANSTON, P. S., OLIVER, D. R. & SÆTHER, O. A., 1983, TRIVINHO-STRIXINO, S. & STRIXINO, G., 1995, Larvas de The larvae of Orthocladiinae (Diptera: Chironomidae) of Chironomidae (Diptera) do Estado de São Paulo: Guia the Holartic region – keys and diagnoses. In: T. Wiederholm de identificação e diagnose dos gêneros. PPGE-RN, (ed.), Chironomidae of the Holartic region. Keys and Universidade Federal de São Carlos, SP, 227p. diagnose. Part I: Larvae. Ent. Scan. Suppl., 19: 149-291. CRANSTON, P. S. & OLIVER, D. R., 1988, Aquatic xylophagous Orthocladiinae – systematics and ecology. Spixiana Suppl., 14: 143-154. CUMMINS, K. W. & KLUG, M. J., 1979, Feeding ecology on

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